DOCSLIB.ORG

Organization and Postembryonic Development of Glial Cells in the Adult Central Brain of Drosophila

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Organization and Postembryonic Development of Glial Cells in the Adult Central Brain of Drosophila 13742 • The Journal of Neuroscience, December 17, 2008 • 28(51):13742–13753 Development/Plasticity/Repair Organization and Postembryonic Development of Glial Cells in the Adult Central Brain of Drosophila Takeshi Awasaki,1* Sen-Lin Lai,1* Kei Ito,2 and Tzumin Lee1 1Department of Neurobiology, University of Massachusetts, Worcester, Massachusetts 01605, and 2Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo 113-0032, Japan Glial cells exist throughout the nervous system, and play essential roles in various aspects of neural development and function. Distinct types of glia may govern diverse glial functions. To determine the roles of glia requires systematic characterization of glia diversity and development. In the adult Drosophila central brain, we identify five different types of glia based on its location, morphology, marker expression, and development. Perineurial and subperineurial glia reside in two separate single-cell layers on the brain surface, cortex glia form a glial mesh in the brain cortex where neuronal cell bodies reside, while ensheathing and astrocyte-like glia enwrap and infiltrate into neuropils, respectively. Clonal analysis reveals that distinct glial types derive from different precursors, and that most adult peri- neurial, ensheathing, and astrocyte-like glia are produced after embryogenesis. Notably, perineurial glial cells are made locally on the brain surface without the involvement of gcm (glial cell missing). In contrast, the widespread ensheathing and astrocyte-like glia derive from specific brain regions in a gcm-dependent manner. This study documents glia diversity in the adult fly brain and demonstrates involvement of different developmental programs in the derivation of distinct types of glia. It lays an essential foundation for studying glia development and function in the Drosophila brain. Key words: glial cells; glial subtype; cell lineage; adult brain; MARCM; Drosophila Introduction model system for studying glial development and function up to Proper development and function of neural circuitry require glial individual cells. Based on the position of glial cell bodies and cells. Although glial cells were originally believed to have just morphology, glial cells in the Drosophila ventral ganglion are supporting roles in nourishing and insulating neurons, recent classified into three types; surface-, cortex-, and neuropil- studies have revealed that glia contribute to virtually all aspects of associated glial cells (Ito et al., 1995). They are derived from nervous system development and function [for review, see Lemke specific neuroglioblasts and glioblasts (Schmidt et al., 1997; (2001), Villegas et al. (2003), and Parker and Auld (2006)]. How- Schmid et al., 1999). The glial cell missing (gcm) gene governs the ever, our understanding of glial diversity and origin is far behind derivation of all embryonic glial cells except for one specific type their neuronal counterparts. of glia, midline glia (Hosoya et al., 1995; Jones et al., 1995; Vin- Drosophila, with its accessibility to genetic, molecular, and cent et al., 1996). Loss of gcm causes deficits in glial production behavior analysis, has emerged as a powerful model system for while ectopic GCM transform neurons to glia. Thus, gcm is nec- studying brain development and function and its underlying mo- essary and sufficient for driving glial development during lecular mechanisms. In contrast to vertebrates, in which neurons embryogenesis. are outnumbered by glial cells, Drosophila have fewer neurons Embryonic glia also play essential roles in regulating neuronal and exhibits a lower glia–neuron ratio with even fewer glial cells viability and morphogenesis. Neuronal loss and connectivity de- (Ito et al., 1995; Pfrieger and Barres, 1995). fects are observed following ablation of glial cells (Booth et al., The larval ventral ganglion constitutes a relatively simple 2000; Hidalgo and Booth, 2000), although survival and func- tional differentiation of glial cells also require signals from neu- rons (Hidalgo et al., 2001). In addition, glial cells located at the Received Oct. 8, 2008; revised Oct. 28, 2008; accepted Nov. 1, 2008. midline, midline glia, secrete and present molecules to guide the This work was supported by Naito Foundation to T.A., a Grant-in-Aid for Scientific Research from the Ministry of growth cone of axons (Kidd et al., 1999). Education, Culture, Sports, Science, and Technology of Japan to K.I., and the United States National Institutes of Defects in glial function affect various adult behaviors of Health to T.L. We are grateful to M. R. Freeman for communicating results before publication; M. R. Freeman and Drosophila, including circadian rhythm, courtship behavior, Bloomington Stock Center for fly strains; G. G. Technau and Developmental Studies Hybridoma Bank for antibodies; H.-H. Yu for sharing UAS-mCD8::RFP strains before publication; the members of Ito’s laboratory for screening of fly and longevity (Ewer et al., 1992; Buchanan and Benzer, 1993; strains; members of Lee’s laboratory for fruitful discussion; and B. Leung for critical reading of this manuscript. Kretzschmar et al., 1997; Suh and Jackson, 2007; Grosjean et al., *T.A. and S.-L.L. contributed equally to this study. 2008). Disruption of glial function in mature brains also induces Correspondence should be addressed to either Takeshi Awasaki or Tzumin Lee at the above address. E-mail: neural degeneration (Xiong and Montell, 1995; Kretzschmar et [email protected] or [email protected]. Sen-Lin Lai’s present address: Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403. al., 1997). In addition, glia play an essential role in the clearance DOI:10.1523/JNEUROSCI.4844-08.2008 of degenerating axons in both pupal and adult brains (Awasaki Copyright © 2008 Society for Neuroscience 0270-6474/08/2813742-12$15.00/0 and Ito, 2004; Watts et al., 2004; Awasaki et al., 2006; Hoopfer et Awasaki et al. • Glial Cells in Adult Drosophila Brain J. Neurosci., December 17, 2008 • 28(51):13742–13753 • 13743 al., 2006; MacDonald et al., 2006). Further elucidation of these Results glial functions and their underlying mechanisms requires better Classification of Repo-positive glial cells in the adult characterization of glial cells in the adult brain and their deriva- Drosophila central brain tion through postembryonic development of the Drosophila In the Drosophila embryonic CNS, glial cells are classified into brain. In this study, we show five different types of glial cells three categories based on the position of their cell bodies, cell locate in the adult fly brain with specific patterns and are pro- morphology, and characteristic labeling pattern of the GAL4 en- duced by distinct developmental programs. hancer trap lines: surface-, cortex-, and neuropil-associated glia (Ito et al., 1995). Except for midline glial cells, which are finally eliminated by apoptosis during the pupal stage, all other glial cells Materials and Methods in the CNS express a homeodomain protein, Repo (Xiong et al., Fly strains. To label specific subtypes of glia, we screened in total ϳ3500 1994; Halter et al., 1995; Awad and Truman, 1997). To analyze GAL4 enhancer trap strains made by NP consortium (NP lines) (Hayashi glial cells in the adult central brain, we therefore focused on the et al., 2002): NP6293 (perineurial glia), NP2276 (subperineurial glia), Repo-positive glial cells. Nuclei of Repo-positive glial cells were NP577 and NP2222 (cortex glia), NP3233 and NP1243 (astrocyte-like observed on the brain surface, in the cortex, and around and glia), and NP6520 (ensheathing glia). Note that although these lines label within neuropils (Fig. 1A,D–F). In addition, when glial mem- specific subtypes of glia preferentially, they are not pure lines exclusively brane were revealed with membrane-tagged GFP (mCD8::GFP) labeling only specific subtype of glia; every line also labels a subset of driven by repo-GAL4, surface, cortex, and neuropils of the adult neurons. NP1243 labels ensheathing glia and cortex glia weakly and brain were labeled (Fig. 1B,C). These observations suggest that NP6520 also labels cortex glia weakly. Two different repo-GAL4 lines were used as pan-glial lines localized on X and third chromosome, respectively glial cells in the adult central brain could also be classified into (Sepp et al., 2001; Lai and Lee, 2006). gcm⌬P1 (Jones et al., 1995) and three categories like those of the larval CNS. Df(2L)132 (Kammerer and Giangrande, 2001) were used for gcm mutant To examine their morphologies, we labeled small subsets of and deletion chromosome uncovering gcm and gcm2, respectively. To glial cells in the adult brain using a UAS-FLP-out system com- make a repo-GAL80 line, GAL80 from tubP-GAL80 (Lee and Luo, 1999) bined with repo-GAL4. On the brain surface, two morphologi- was subcloned into pCaSpeR4 vector, which carries the repo-promoter cally different types of glial cells were identified (Fig. 1G,H). One (Lai and Lee, 2006), and transgenic flies were generated with this con- was a small and slender oblong cell and the other was a large struct. (1) hs-FLP; UAS-FRT-rCD2-FRT-mCD8::GFP was used for FLP- sheet-like cell. These two types of glial cells were present through- out labeling. (2) hs-FLP; FRTG13, tubP-GAL80, repo-GAL80/CyO, (3) out the entire brain surface. In the cortex region, cells with mesh- repo-GAL4; G13, UAS-mCD8::GFP/CyO, and (4) repo-GAL4; G13, UAS- like morphology were evident (Fig. 1I). Each mesh-like cell oc- nlsGFP/CyO were used for systematic MARCM analysis of glia. (5) gcm- cupies a distinct part of brain cortex. Although cells labeled in the GAL4, FRTG13, UAS-nlsGFP/CyO was used for MARCM analysis of brain cortex possessed a common mesh-like structure, the size of gcm-expressing cells. (6) repo-GAL4; FRT40A, tubP-GAL80/CyO; UAS- each cell varied. In the neuropil region, two types of glial cells ⌬P1 nlsGFP/TM3 Sb, (7) hs-FLP; FRT40A, (8) hs-FLP; FRT40A, gcm /CyO, were revealed (Fig.
Load more

Recommended publications
  • In Vivo Imaging of Microglia-Mediated Axonal Pruning and Modulation By
    Combined bioRxivsingle preprintmanuscript doi: https://doi.org/10.1101/2020.06.07.087221 file ; this version posted June 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 In vivo imaging of microglia-mediated axonal pruning and modulation 2 by the complement system 3 Tony K.Y. Lim1 and Edward S. Ruthazer1,2,* 4 1. Department of Neurology & Neurosurgery, Montreal Neurological Institute-Hospital, McGill 5 University, Montreal, Quebec, H3A 2B4; Canada 6 2. Lead Contact 7 *Correspondence: [email protected] 8 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.07.087221; this version posted June 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 9 Summary 10 Partial phagocytosis – called trogocytosis – of axons by microglia has been documented in ex vivo 11 preparations but has yet to be observed in vivo. Fundamental questions regarding the mechanisms that 12 modulate axon trogocytosis as well as its function in neural circuit development remain unanswered. 13 Here we used 2-photon live imaging of the developing Xenopus laevis retinotectal circuit to observe 14 axon trogocytosis by microglia in vivo. Amphibian regulator of complement activation 3 (aRCA3) was 15 identified as a neuronally expressed, synapse-associated complement inhibitory molecule. 16 Overexpression of aRCA3 enhanced axonal arborization and inhibited trogocytosis, while expression of 17 VAMP2-C3, a complement-enhancing fusion protein tethered to the axon surface, reduced axonal 18 arborization.
    [Show full text]
  • Microglia Control Glutamatergic Synapses in the Adult Mouse Hippocampus
    bioRxiv preprint doi: https://doi.org/10.1101/2021.02.01.429096; this version posted February 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Microglia control glutamatergic synapses in the adult mouse hippocampus Short title: Microglia and glutamatergic synapses Bernadette Basilico1†*‡, Laura Ferrucci1‡, Patrizia Ratano2‡, Maria T. Golia1, Alfonso Grimaldi3, Maria Rosito3, Valentina Ferretti4, Ingrid Reverte1,5, Maria C. Marrone6, Maria Giubettini3,7, Valeria De Turris3, Debora Salerno3, Stefano Garofalo1, Marie-Kim St-Pierre8, Micael Carrier8, Massimiliano Renzi1, Francesca Pagani3, Marcello Raspa9, Ferdinando Scavizzi9, Cornelius T. Gross10, Silvia Marinelli5, Marie E. Tremblay8,11, Daniele Caprioli1,5, Laura Maggi1, Cristina Limatola1,2, Silvia Di Angelantonio1,3§, Davide Ragozzino1,5*§ 1Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy. 2IRCCS Neuromed, Via Atinese 18, 86077, Pozzilli, IS, Italy. 3Center for Life Nanoscience, Istituto Italiano di Tecnologia, Rome, Italy. 4Dipartimento di Biologia e Biotecnologie "Charles Darwin", Sapienza University of Rome, Rome, Italy. 5Santa Lucia Foundation (IRCCS Fondazione Santa Lucia), Rome, Italy. 6European Brain Research Institute-Rita Levi Montalcini, Rome, Italy. 7CrestOptics S.p.A., Via di Torre Rossa 66, 00165 Rome, Italy. 8Centre de Recherche du CHU de Québec, Axe Neurosciences Québec, QC, Canada; Département de médecine moléculaire, Université Laval Québec, QC, Canada. 9National Research Council, Institute of Biochemistry and Cell Biology (CNR- IBBC/EMMA/Infrafrontier/IMPC), International Campus “A. Buzzati-Traverso”, Monterotondo (Rome) Italy.
    [Show full text]
  • Neuroglial Response to Neuron Injury. a Study Using Intraneural Injection of Ricinus Communis Agglutinin-60
    J. Anat. (1989), 164, pp. 201-213 201 With 16 figures Printed in Great Britain Neuroglial response to neuron injury. A study using intraneural injection of ricinus communis agglutinin-60 E. A. LING, C. Y. WEN*, J. Y. SHIEH*, T. Y. YICK AND S. K. LEONG Department of Anatomy, Faculty of Medicine, National University of Singapore, Singapore 0511 and * Department of Anatomy, College of Medicine, National Taiwan University, Taipei, Taiwan 10018 (Accepted 27 September 1988) INTRODUCTION Several studies have shown that ricinus communis agglutinin (RCA), when injected into a nerve in minute amounts, is retrogradely transported by axons in the nerve, resulting in a selective destruction of the parental cell bodies. Thus, the administration of RCA into the vagus nerve would cause a selective destruction of the efferent neurons in the dorsal motor nucleus (Wiley, Blessing & Reis, 1982; Ling & Leong, 1987, 1988). Such a 'suicide transport' of the toxic lectin is also evident in sensory neurons (Yamamoto, Iwasaki & Konno, 1983, 1984; Johnson, Westrum, Henry & Canfield, 1985; Wiley & Oeltmann, 1986). Recently, the use of RCA has become increasingly important as a research tool for tracing the central projections of primary afferents of peripheral nerves (Yamamoto et al. 1983; Leong & Tan, 1987; Ling & Leong, 1987). While much is known about the consequent death of neurons following RCA application, little is known about the response of the non-neuronal cells either closely associated with, or in the vicinity of, the degenerating neurons. According to Yamamoto et al. (1984), the selective destruction of neurons in the trigeminal and dorsal root ganglia by RCA could possibly stimulate the capsule cells involved in the phagocytosis of the degenerating nerve cells.
    [Show full text]
  • University International
    INFORMATION TO USERS This was produced from a copy of a document sent to us for microfilming. While the most advanced technological means to photograph and reproduce this document have been used, the quality is heavily dependent upon the quality of the material submitted. The following explanation of techniques is provided to help you understand markings or notations which may appear on this reproduction. 1. The sign or “target” for pages apparently lacking from the document photographed is “Missing Page(s)”. If it was possible to obtain the missing page(s) or section, they are spliced into the film along with adjacent pages. This may have necessitated cutting through an image and duplicating adjacent pages to assure you of complete continuity. 2. When an image on the film is obliterated with a round black mark it is an indication that the film inspector noticed either blurred copy because of movement during exposure, or duplicate copy. Unless we meant to delete copyrighted materials that should not have been filmed, you will find a good image of the page in the adjacent frame. 3. When a map, drawing or chart, etc., is part of the material being photo­ graphed the photographer has followed a definite method in “sectioning” the material. It is customary to begin filming at the upper left hand corner of a large sheet and to continue from left to right in equal sections with small overlaps. If necescary, sectioning is continued again—beginning below the first row and continuing on until complete. 4. For any illustrations that cannot be reproduced satisfactorily by xerography, photographic prints can be purchased at additional cost and tipped into your xerographic copy.
    [Show full text]
  • The Functional Organization of Descending Sensory-Motor 2 Pathways in Drosophila 3 4 5 Shigehiro Namiki,1 Michael H
    bioRxiv preprint doi: https://doi.org/10.1101/231696; this version posted December 11, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 The functional organization of descending sensory-motor 2 pathways in Drosophila 3 4 5 Shigehiro Namiki,1 Michael H. Dickinson,2 Allan M. Wong,1 Wyatt Korff,1 Gwyneth M. 6 Card,1,* 7 8 1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147, USA 9 2Division of Biology and Bioengineering, California Institute of Technology, Pasadena, CA 91125, USA 10 11 12 This manuscript includes 55 pages of typescript, 15 figures, 0 tables, 24 supplemental figures, and 6 13 supplementary tables. 14 15 KEYWORDS: command neuron; descending neuron; motor control; neuron database; ventral 16 nervous system 17 18 *Correspondence should be addressed to [email protected] (G.M.C) 19 1 bioRxiv preprint doi: https://doi.org/10.1101/231696; this version posted December 11, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 20 SUMMARY 21 22 In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck 23 and terminate in post-cranial regions of the nervous system. This critical neural population is thought to 24 activate, maintain and modulate locomotion and other behaviors. Although individual members of this 25 cell class have been well-studied across species ranging from insects to primates, little is known about the 26 overall connectivity pattern of DNs as a population.
    [Show full text]
  • Structural and Developmental Principles of Neuropil Assembly in C
    Article Structural and developmental principles of neuropil assembly in C. elegans https://doi.org/10.1038/s41586-020-03169-5 Mark W. Moyle1, Kristopher M. Barnes2, Manik Kuchroo3, Alex Gonopolskiy3, Leighton H. Duncan1, Titas Sengupta1, Lin Shao1, Min Guo4, Anthony Santella2, Received: 21 April 2020 Ryan Christensen4, Abhishek Kumar5, Yicong Wu4, Kevin R. Moon6, Guy Wolf7, Accepted: 12 November 2020 Smita Krishnaswamy3,10, Zhirong Bao2,10, Hari Shroff4,5,10, William A. Mohler8,10 & Daniel A. Colón-Ramos1,5,9,10 ✉ Published online: xx xx xxxx Check for updates Neuropil is a fundamental form of tissue organization within the brain1, in which densely packed neurons synaptically interconnect into precise circuit architecture2,3. However, the structural and developmental principles that govern this nanoscale precision remain largely unknown4,5. Here we use an iterative data coarse-graining algorithm termed ‘difusion condensation’6 to identify nested circuit structures within the Caenorhabditis elegans neuropil, which is known as the nerve ring. We show that the nerve ring neuropil is largely organized into four strata that are composed of related behavioural circuits. The stratifed architecture of the neuropil is a geometrical representation of the functional segregation of sensory information and motor outputs, with specifc sensory organs and muscle quadrants mapping onto particular neuropil strata. We identify groups of neurons with unique morphologies that integrate information across strata and that create neural structures that cage the strata within the nerve ring. We use high resolution light-sheet microscopy7,8 coupled with lineage-tracing and cell-tracking algorithms9,10 to resolve the developmental sequence and reveal principles of cell position, migration and outgrowth that guide stratifed neuropil organization.
    [Show full text]
  • Oligodendrocyte Precursor Cells Sculpt the Visual System by Regulating Axonal Remodeling
    bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434829; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Oligodendrocyte Precursor Cells Sculpt the Visual System by Regulating 2 Axonal Remodeling 3 4 Yan Xiao1, Laura J Hoodless2, Luigi Petrucco3,4, Ruben Portugues2,4,5, Tim Czopka1,2,5 5 1) Institute of Neuronal Cell Biology, Technical University of Munich, Germany 6 2) Centre for Clinical Brain Sciences, University of Edinburgh, United Kingdom 7 3) Max Planck Institute of Neurobiology, Sensorimotor Control Research Group, Martinsried 82152, 8 Germany 9 4) Institute of Neuroscience, Technical University of Munich, Germany 10 5) Munich Cluster for Systems Neurology (SyNergy), Germany 11 12 13 *Correspondence to 14 15 Dr. Tim Czopka 16 University of Edinburgh 17 Centre for Clinical Brain Sciences 18 Chancellor's Building 19 49 Little France Crescent 20 Edinburgh EH16 4SB, United Kingdom 21 [email protected] bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434829; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 22 Abstract 23 Many oligodendrocyte precursor cells (OPCs) do not differentiate to form myelin, suggesting 24 additional roles of this cell population.
    [Show full text]
  • Characterization of Oligodendrocyte Lineage Precursor Cells in the Mouse Cerebral Cortex: a Confocal Microscopy Approach to Demyelinating Diseases
    IJAE Vol. 115, n. 1/2: 95-102, 2010 ITALIAN JOURNAL OF ANATOMY AND EMBRYOLOGY Characterization of oligodendrocyte lineage precursor cells in the mouse cerebral cortex: a confocal microscopy approach to demyelinating diseases Francesco Girolamo*, Maurizio Strippoli, Mariella Errede, Vincenzo Benagiano, Luisa Roncali, Glauco Ambrosi, Daniela Virgintino Dipartimento di Anatomia Umana e di Istologia ‘Rodolfo Amprino’, Facoltà di Medicina e Chirurgia – Policlinico – Università di Bari, Italia. *Corresponding author, Email: [email protected] Presented at a meeting in honour of Prof. G. Orlandini, Florence, February 15, 2010 Summary The identifi cation of stem cells resident in the adult central nervous system has redirected the focus of research into demyelinating diseases, such as multiple sclerosis, mainly affecting the brain white matter. This immunocytochemical and morphometrical study was carried out by confocal microscopy in the adult mouse cerebral cortex, with the aim of analysing, in the brain grey matter, the characteristics of the oligodendrocyte lineage cells, whose capability to remyeli­ nate is still controversial. The observations demonstrated the presence in all the cortex layers of glial restricted progenitors, reactive to A2B5 marker, oligodendrocyte precursor cells, expressing the NG2 proteoglycan, and pre­oligodendrocytes and pre­myelinating oligodendrocytes, reac­ tive to the specifi c marker O4. NG2 expressing cells constitute the major immature population of the cortex, since not only oligodendrocyte precursor cells and pre­oligodendrocytes but also a part of the glial restrict progenitors express the NG2 proteoglycan. Together with the popula­ tion of these immature cells, a larger population of mature oligodendrocytes was revealed by the classical oligodendrocyte and myelin markers, 2’,3’­cyclic nucleotide 3’­phosphodiesterase, myelin basic protein and myelin oligodendrocyte glycoprotein.
    [Show full text]
  • Mechanosensation and Adaptive Motor Control in Insects
    Current Biology Review Mechanosensation and Adaptive Motor Control in Insects John C. Tuthill1 and Rachel I. Wilson2 1Department of Physiology and Biophysics, University of Washington, 1705 NE Pacific Street, Seattle, WA 98195, USA 2Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA Correspondence: [email protected] (J.C.T.), [email protected] (R.I.W.) http://dx.doi.org/10.1016/j.cub.2016.06.070 The ability of animals to flexibly navigate through complex environments depends on the integration of sen- sory information with motor commands. The sensory modality most tightly linked to motor control is mecha- nosensation. Adaptive motor control depends critically on an animal’s ability to respond to mechanical forces generated both within and outside the body. The compact neural circuits of insects provide appealing sys- tems to investigate how mechanical cues guide locomotion in rugged environments. Here, we review our cur- rent understanding of mechanosensation in insects and its role in adaptive motor control. We first examine the detection and encoding of mechanical forces by primary mechanoreceptor neurons. We then discuss how central circuits integrate and transform mechanosensory information to guide locomotion. Because most studies in this field have been performed in locusts, cockroaches, crickets, and stick insects, the exam- ples we cite here are drawn mainly from these ‘big insects’. However, we also pay particular attention to the tiny fruit fly, Drosophila, where new tools are creating new opportunities, particularly for understanding cen- tral circuits. Our aim is to show how studies of big insects have yielded fundamental insights relevant to mechanosensation in all animals, and also to point out how the Drosophila toolkit can contribute to future progress in understanding mechanosensory processing.
    [Show full text]
  • Neural Coding of Leg Proprioception in Drosophila
    bioRxiv preprint doi: https://doi.org/10.1101/274498; this version posted March 9, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Neural coding of leg proprioception in Drosophila Akira Mamiya1, Pralaksha Gurung1, and John Tuthill1* 1Department of Physiology and Biophysics, University of Washington 98195 *Correspondence: [email protected] Summary Animals rely on an internal sense of body position and movement to effectively control motor behavior. This sense of proprioception relies on diverse populations of mechanosensory neurons distributed throughout the body. However, little is known about how proprioceptor neurons collectively encode sensory stimuli. Here, we investigate neural coding of leg proprioception in Drosophila, using in vivo two-photon calcium imaging of proprioceptors during controlled movements of the fly tibia. We found that the axons of leg proprioceptors are organized into distinct functional projections that contain topographic representations of specific kinematic features. Using subtype-specific genetic driver lines, we show that one group of axons encodes tibia position (flexion/extension), another encodes movement direction, and a third encodes bidirectional movement and vibration frequency. Thus, proprioceptive sensing of a single leg joint is mediated by multiple subtypes of specialized sensory neurons. This architecture may help to maximize information transmission, processing speed, and robustness, which are critical for feedback control of the limbs during locomotion. Introduction Proprioception, the internal sense of body position and movement (Sherrington, 1906), is essential for the neural control of motor behavior.
    [Show full text]
  • Microglia Depletion-Induced Remodeling of Extracellular Matrix and Excitatory Synapses in the Hippocampus of Adult Mice
    cells Article Microglia Depletion-Induced Remodeling of Extracellular Matrix and Excitatory Synapses in the Hippocampus of Adult Mice Luisa Strackeljan 1, Ewa Baczynska 2 , Carla Cangalaya 1,3,4, David Baidoe-Ansah 1 , Jakub Wlodarczyk 2, Rahul Kaushik 1,* and Alexander Dityatev 1,5,6,* 1 Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany; [email protected] (L.S.); [email protected] (C.C.); [email protected] (D.B.-A.) 2 Nencki Institute of Experimental Biology, Polish Academy of Sciences, Pasteura 3, 02-093 Warsaw, Poland; [email protected] (E.B.); [email protected] (J.W.) 3 Institut für Biochemie und Zellbiologie, Medical Faculty, Otto-von-Guericke-University, 39120 Magdeburg, Germany 4 ESF International Graduate School on Analysis, Imaging and Modelling of Neuronal and Inflammatory Processes, 39120 Magdeburg, Germany 5 Center for Behavioral Brain Sciences (CBBS), 39106 Magdeburg, Germany 6 Medical Faculty, Otto-von-Guericke University, 39120 Magdeburg, Germany * Correspondence: [email protected] (R.K.); [email protected] (A.D.); Tel.: +49-391-67-24526 (A.D.); Fax: +49-391-6724530 (A.D.) Citation: Strackeljan, L.; Abstract: The extracellular matrix (ECM) plays a key role in synaptogenesis and the regulation of Baczynska, E.; Cangalaya, C.; Baidoe-Ansah, D.; Wlodarczyk, J.; synaptic functions in the central nervous system. Recent studies revealed that in addition to dopamin- Kaushik, R.; Dityatev, A. Microglia ergic and serotoninergic neuromodulatory systems, microglia also contribute to the regulation of Depletion-Induced Remodeling of ECM remodeling. In the present work, we investigated the physiological role of microglia in the re- Extracellular Matrix and Excitatory modeling of perineuronal nets (PNNs), predominantly associated with parvalbumin-immunopositive Synapses in the Hippocampus of (PV+) interneurons, and the perisynaptic ECM around pyramidal neurons in the hippocampus.
    [Show full text]
  • The Function of Dendritic Spines: Devices Subserving Biochemical Rather Than Electrical Compartmentalization
    The Journal of Neuroscience, February 1993, 13(2): 413422 Feature Article The Function of Dendritic Spines: Devices Subserving Biochemical Rather Than Electrical Compartmentalization Christof Koch’ and Anthony Zador* ‘Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125 and *Neuroscience Program, Yale University School of Medicine, New Haven, Connecticut 06510 Dendritic spines are tiny, specialized protoplasmic protuber- (2) spinesshape the membranepotential in responseto synaptic ances that cover the surface of many neurons. First described input, and (3) spinesdetermine the dynamics of intracellular by Ramon y Cajal(199 1) in light microscopic studies of Golgi- second messengerssuch as calcium. In this article we review stained tissue, they are among the most striking subcellular fea- the current status of each of these proposals with particular tures of many neurons. Spines serve as the major target for emphasison the putative role of spinesin the induction of a excitatory synaptic input onto principal neurons in the hippo- cellular model of synaptic plasticity in cortical structures, long- campus, the neocortex, and other brain regions. Their intimate term potentiation (LTP). association with synaptic traffic suggests some critical role in It may well be possiblethat dendritic spinesserve somecrucial synaptic transmission and plasticity. We here review experi- role in normal synaptic transmission(D. Purves, personalcom- mental data and theoretical models with respect to the putative
    [Show full text]